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Reentrant phase transformation from crystalline † Cite this: CrystEngComm,2018,20, ikaite to amorphous calcium carbonate 2902 Zhaoyong Zou, Luca Bertinetti, Wouter J. E. M. Habraken and Peter Fratzl * Received 2nd February 2018, Accepted 13th April 2018

DOI: 10.1039/c8ce00171e

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We report the spontaneous transformation of highly hydrated massive creation of defects.5,6 It can also be caused by hydro- crystalline ikaite into less hydrated amorphous calcium carbonate genation of intermetallics where hydrogen atoms in crystal- (ACC), which has the outer contours of micrometer-sized crystals, line phases are less energetically favourable.7 In addition, de- a multi-level interconnected porous structure and a very high spe- hydration of crystalline hydrates has been demonstrated as a cific surface area (98.3 cm2 g−1). The ikaite was previously obtained route to the amorphous state of several organic solids5 or Creative Commons Attribution 3.0 Unported Licence. by transformation of an uncommon hydrated ACC with as much copper sulphate pentahydrate.8 Finally, crystalline coordina-

H2O as ikaite, synthesized at 2 °C without any additives. The solid- tion networks or highly porous metal–organic frameworks be- state amorphization was induced by the fast dehydration of the come amorphous upon losing constitutional solvent crystal. molecules.9,10 Ikaite is a highly hydrated crystalline calcium carbonate According to the well-known Ostwald rule,1 thermodynami- phase (CaCO3·6H2O) containing discrete CaCO3 ion pairs cally less stable phases appearing first in a precipitate from each surrounded by an envelope of 18 water molecules.11 The solution further transform into more stable phases until the neighbouring ion pairs are linked by hydrogen bonds only, most stable crystalline phase is formed. In general, amor- 12 This article is licensed under a which are temperature sensitive. Therefore, ikaite is only phous materials as the most unstable solid states would typi- stable at temperatures below 5 °C and in the natural environ- 2,3 cally transform into more stable crystalline phases. In the ment it is only found in cold seawater, deep-sea sediment, case of calcium carbonate, for example, amorphous calcium

Open Access Article. Published on 18 April 2018. Downloaded 9/27/2021 10:55:12 PM. carbonate (ACC) has been widely observed as a transient precursor for the formation of crystalline calcium carbonate bio- minerals.4 Here, we report that the opposite transformation from a crystalline calcium carbonate phase into ACC can also happen spontaneously. Solid state amorphization, a process where a crystalline phase transforms into an amorphous state, may happen through a large input of energy necessary for such an energetically “uphill” conversion of structures. A typical example is mechanical grinding of crystalline materials, which may lead to amorphous materials via generation of localized heating followed by quenching, via an increase in disorder or

Max Planck Institute of Colloids and Interfaces, Potsdam, 14476, Germany. E-mail: [email protected] Fig. 1 (a) The evolution of pH and calcium activity (indicated by the † Electronic supplementary information (ESI) available: Detailed experimental measured potential from a calcium electrode) of the reaction solution. procedures, characterization of the ikaite sample after filtration, TGA curves of (b) The FTIR spectra of ACC and ikaite measured directly after different ACC samples, FTIR spectra of different ACC samples, morphology of filtration. (c) The TGA curves of ACC and ikaite where the temperature the ACC transformed from ikaite and SAXS analysis of the sample under heating was maintained at 20 °C for 25 min before they were heated to 300 °C − (PDF), and a video of the ACC investigated by FIB/SEM (mpg). See DOI: 10.1039/ at a rate of 1.5 °C min 1. The SEM images of ACC (d) and a sample c8ce00171e during transformation (∼2400 s, ACC + ikaite) (e).

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and cold spring water where the temperature is near high mobility of water in the structure of ACC where the ma- 0 °C.13,14 At elevated temperatures, it usually transforms into jority of water can be easily removed at room temperature un- thermodynamically more stable calcite or vaterite, with the der vacuum. characteristic shape of ikaite preserved.15,16 However, the To understand how ACC transforms into ikaite, the mor- mechanism that governs these transformation processes is phology of samples during transformation was investigated. not clear. The scanning electron microscopy (SEM) images show that In this study, we aim at understanding the mechanisms the ACC nanoparticles (Fig. 1d) are spherical in shape with for the unusual transformation of crystalline ikaite to ACC. an average diameter of 69 ± 27 nm. For the sample taken dur- We find that ikaite can first be obtained by the transforma- ing transformation (Fig. 1e), there are many nanoparticles

tion of ACC with more than 6 H2O per CaCO3 in solution at less than 30 nm attaching onto the surface of large ikaite 2 °C. More interestingly, we find that fast dehydration of crystals. These nanoparticles are clearly much smaller than this crystalline ikaite can induce its subsequent transforma- the ACC precursor, suggesting that the ACC precursor is only tion into less hydrated ACC with a multi-level inter- partially dissolved and decomposed into these smaller nano- connected porous structure with a high specific surface particles. Afterwards, these nanoparticles attach onto the sur- area. Our findings show that a hydrated crystal can be face of ikaite crystals and seem to transform into ikaite via lo- converted into an amorphous solid just by sufficiently fast cal dissolution–recrystallization. This phenomenon is similar removal of water. to the transformation process from ACC to vaterite and cal- Using the procedure described in a previous study,17 the cite in a pure system, as observed in a previous study.17 formation of ACC and its transformation into ikaite are inves- It is well known that ikaite is very unstable at room tem- 15,16 tigated by adding 0.5 mL 1 M CaCl2 solution into 49.5 mL perature and can easily transform into vaterite or calcite.

20.2 mM Na2CO3 solution at 2 °C under stirring. In situ pH However, surprisingly, here we found that ikaite can easily and calcium activity measurements (Fig. 1a) suggest that ACC transform into ACC in air with low humidity or under

Creative Commons Attribution 3.0 Unported Licence. precipitates immediately after the addition of CaCl2 solution vacuum. at 120 s and it remains stable in the mother solution for The transformation of ikaite in air was measured in situ ∼2000 s before it transforms into crystalline calcium carbon- by XRD (Fig. 2a), which shows that the intensity of the sharp ate with lower solubility.17 Samples are collected at different Bragg diffraction peaks of ikaite gradually decreases with stages of the reaction by vacuum filtration of the solution time and finally only two broad humps corresponding to ACC and washing with ethanol to remove the surface water. The could be observed. The transformation under vacuum was in- infrared spectra of the samples (Fig. 1b) confirm that the ini- vestigated by infrared spectroscopy (Fig. 2b), which shows tial precipitate is amorphous and show that the one after that the peak corresponding to the out-of-plane bending ν −1 crystallization is pure ikaite, which is further confirmed by mode 2 of the carbonate group shifts from 872 cm to 862

This article is licensed under a − XRD and Raman analysis (Fig. S1†). The similar relative cm 1 and becomes sharper, while the in-plane bending mode −1 intensities of the peaks corresponding to the OH stretching ν4 of the carbonate group at 671 cm shifts to a higher −1 −1 −1 at 3320 cm and the H2O bending at 1646 cm for the as- wavenumber at 694 cm and becomes broader, confirming

Open Access Article. Published on 18 April 2018. Downloaded 9/27/2021 10:55:12 PM. synthesized ACC and ikaite suggest that both samples con- the transformation from ikaite to ACC without any other crys- tain similar amounts of water. The water contents are deter- talline phases. Interestingly, while the asymmetric stretching ν mined by performing thermogravimetric analysis (TGA), mode 3 of the carbonate group gradually evolves into a where the sample is first maintained at 20 °C under a nitro- shape corresponding to ACC with two splitting peaks, the po- − − gen flow (20 mL min 1) for 25 min and then heated at a rate sition of the main peak remains at 1392 cm 1, which is sig- − of 1.5 °C min 1. As shown in Fig. 1c, both samples dehydrate nificantly lower than the typical values for both synthetic quickly even at 20 °C, and the average weight loss after 300 (Fig. S3†) and biogenic ACC samples (between 1406 and 1417 − °C is 52.7 ± 2.0% for the as-synthesized ACC and 50.4 ± 1.6% cm 1).17,18 This suggests that the local atomic structure of · for ikaite, corresponding to a composition of CaCO3 6.2H2O this ACC is different from the ACC formed from solution. and CaCO3·5.6H2O, respectively. Within the experimental er- ror, the water content of ikaite corresponds to the known 11 value of 6 H2O molecules per CaCO3. Interestingly, the water content of the as-synthesized ACC is of the same order,

an unusually high value as compared to roughly one H2O

molecule per CaCO3 for both biogenic and synthetic ACC – according to previous studies.18 22 It should be noted that if the as-synthesized ACC sample is further dried under vac- ∼ uum, it contains only 0.8 H2O molecules per CaCO3 (Fig. S2†). As a comparison, the ACC synthesized at room tempera-

ture often contains less than 2 H2O molecules per CaCO3 af- ∼ ter filtration and 1.1 H2O molecules per CaCO3 after further Fig. 2 (a) XRD patterns of the ikaite measured in situ in air at room drying under vacuum. These results clearly demonstrate the temperature. (b) FTIR spectra of the ikaite stored under vacuum.

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Since ikaite has 6 H2O per CaCO3 and the ACC obtained

from ikaite transformation under vacuum has only 0.6 H2O per CaCO3, ∼90% of the water is expelled out of the crystal. − Using the densities of ikaite (1.82 g cm 3)23 and ACC (2.43 g − cm 3),24 the volume fraction corresponding to the loss of water should be ∼58%. However, the SEM image (Fig. 3c) of ACC shows that the external shape of ikaite crystals is preserved, but there are many cracks on the surface, suggesting that ACC is highly porous. To understand the transformation process, the nanostructure of ACC was further investigated by focused ion beam/scanning electron microscopy (FIB/SEM). Interestingly, results show that ACC is composed of a huge amount of pores and channels hundreds of nanometers in size (Fig. 3d and S4 and Video S1†), which are interconnected and also connected to the cracks observed on the surface. However, the volume fraction of the pores and channels esti- mated from the analysis of the image stacks is only ∼26%, suggesting the existence of even smaller pores. To investigate this further, the sample was also measured by nitrogen ad- Fig. 4 TGA/DSC curves of the ikaite sample under heating at 3 °C −1 I × q2 sorption and the data were analysed with the Brunauer– min (a) and the corresponding WAXS (b) and SAXS (Kratky plot, vs. q) (c) patterns. The solid arrows on the right indicate the phase Emmett–Teller (BET) method (Fig. 3a and b). The analysis transformation during heating and the dashed arrow indicates that shows an isotherm with a high sorption capacity at a relative ikaite is transformed from ACC in solution. Note that the slight ∼ Creative Commons Attribution 3.0 Unported Licence. pressure (P/P0)of 0.5, revealing the presence of abundant differences in the decomposition temperature from the TGA/DSC and mesopores, which are characterized by a specific surface area WAXS/SAXS data could be due to the different heating set-ups and the − of 98.3 m2 g 1 and an average pore diameter of 3.96 nm. The rate of the N2 flow. − cumulative pore volume is 0.10 cm3 g 1, corresponding to a volume fraction of ∼24%. Thus, the volume fraction of all − − the pores is ∼50%, which fits quite well to the theoretical at 200 ml min 1 for TGA/DSC measurement and 1 L min 1 value by assuming that all these pores are caused by the loss for WAXS/SAXS analysis to remove water as fast as possible. of water during transformation. The TGA/DSC curves (Fig. 4a) show a strong endothermic To describe the dynamics of dehydration and phase trans- peak at 65 °C with more than 80% total weight loss, which is This article is licensed under a formation of ikaite under heating, TGA/DSC and in situ SAXS followed by an exothermic peak at 127 °C and a second stage and WAXS analyses were performed at a heating rate of 3 °C of weight loss. Correspondingly, the WAXS patterns (Fig. 4b) − min 1. To avoid water-induced crystallization of calcite or show that the crystal structure of ikaite is maintained until

Open Access Article. Published on 18 April 2018. Downloaded 9/27/2021 10:55:12 PM. vaterite on the surface of ikaite crystals, the N2 flow was set being heated to ∼55 °C, and then ikaite quickly transforms into ACC. ACC remains stable until ∼130 °C and gradually transforms into a mixture of calcite and vaterite, instead of only calcite, as observed in previous studies.17,25 After 350 °C, the intensity of the vaterite peaks slightly decreases, suggesting that vaterite further transforms into calcite. Corre- spondingly, a strong SAXS signal with a sharp peak at q = 0.8 − nm 1 (7.8 nm in real space) and a broad hump at q = 2.0 − nm 1 (3.1 nm in real space) appears after the decomposition of ikaite (Fig. 4c and S5a†). The intensity of the two peaks further increases upon increasing the temperature to 75 °C, while the sample remains amorphous, suggesting the formation of additional pores. During the crystallization of ACC into vaterite and calcite, the intensity of both peaks decreases very quickly. In addition, according to the linear fitting of the Porod plot (Fig. S5b†), the internal surface area increases quickly during the decomposition of ikaite and then slowly decreases during further crystallization of ACC. Fig. 3 N2 adsorption/desorption isotherms at 77 K (a) and the Based on the above analysis, a clear picture of how ikaite corresponding differential pore volume distribution (Dv(d)) plot (b) of an ACC sample transformed from ikaite under vacuum. Backscattered transforms into ACC can be deduced. It is known that crystal- SEM images showing the surface of ACC (c) and its cross-section after line ikaite consists of discrete CaCO3 ion pairs separated by FIB milling (d). water molecules and these ion pairs are joined by hydrogen

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bonds only, which are the only forces enabling ikaite to Projektkooperation DIP. Zhaoyong Zou was supported by the maintain its crystallinity.13,26,27 As ikaite dehydrates sponta- China Scholarship Council (CSC). Open Access funding pro- neously at room temperature,28 the rapid removal of water vided by the Max Planck Society. molecules results in the breakdown of hydrogen bonds, and the crystalline structure collapses to form an amorphous

solid because the separated CaCO3 units cannot easily References rearrange themselves into a more stable crystalline phase in the solid-state. While such behaviour is known for metal–or- 1 W. Ostwald, Z. Phys. Chem., 1897, 22, 289–330. ganic frameworks,9,10 it is interesting to see that it may also 2 N. D. Loh, S. Sen, M. Bosman, S. F. Tan, J. Zhong, C. A. occur for simple ionic compounds. However, if the dehydra- Nijhuis, P. Král, P. Matsudaira and U. Mirsaidov, Nat. Chem., tion process is not fast enough, heterogeneous nucleation of 2016, 9,77–82. calcite or vaterite occurs. Previous studies have shown that 3 W. J. E. M. Habraken, J. Tao, L. J. Brylka, H. Friedrich, L. moisture on the surface of ikaite accelerates its transforma- Bertinetti, A. S. Schenk, A. Verch, V. Dmitrovic, P. H. H. tion to calcite at cool temperature (13 °C) and rapid transfor- Bomans, P. M. Frederik, J. Laven, P. van der Schoot, B. mation to vaterite is favoured at room temperature.13 This Aichmayer, G. de With, J. J. DeYoreo and N. A. J. M. suggests that kinetic factors such as temperature and the Sommerdijk, Nat. Commun., 2013, 4, 1507. presence of water are critical in controlling the phase trans- 4 S. Weiner and L. Addadi, Annu. Rev. Mater. Res., 2011, 41, formation of ikaite. Therefore, when ikaite crystals are 21–40. washed with ethanol and exposed to air with low humidity, 5 T. Einfalt, O. Planinšek and K. Hrovat, Journal, 2013, 63, water adsorption on the surface is significantly inhibited and 305. heterogeneous nucleation of calcite or vaterite is prevented. 6 J. F. Willart and M. Descamps, Mol. Pharmaceutics, 2008, 5, Recently, Dieckmann et al.29 accidentally found the decompo- 905–920. 231 Creative Commons Attribution 3.0 Unported Licence. sition of ikaite crystals into ACC when they mistakenly stored 7 K. Aoki and T. Masumoto, J. Alloys Compd., 1995, , the crystals in absolute ethanol (>99.9%), rather than in 50% 20–28. ethanol. Apparently, this is also because of the rapid dehydra- 8 G. A. Specken and K. J. McCallum, Nature, 1960, 185, 758. tion of ikaite in pure ethanol. Therefore, our results demon- 9 K. Ohara, J. Martí-Rujas, T. Haneda, M. Kawano, D. strate that the rapid dehydration of ikaite promotes its trans- Hashizume, F. Izumi and M. Fujita, J. Am. Chem. Soc., formation into ACC and the formation of nanocavities within 2009, 131, 3860–3861. the solid while the crystal shape of ikaite is preserved. This is 10 S. Kitagawa, R. Kitaura and S. i. Noro, Angew. Chem., Int. Ed., very interesting because ACC usually forms spherical parti- 2004, 43, 2334–2375. cles, whereby here we show that such a solid-state 11 B. Dickens and W. E. Brown, Inorg. Chem., 1970, 9, 480–486. This article is licensed under a amorphization process can produce ACC resembling the pre- 12 I. P. Swainson and R. P. Hammond, Mineral. Mag., 2003, 67, cursor ikaite particles and may be used in the future to con- 555–562. trol the size and morphology of ACC deposits. 13 T. Ito, Geochem. J., 1998, 32, 267–273.

Open Access Article. Published on 18 April 2018. Downloaded 9/27/2021 10:55:12 PM. To summarize, here we discovered that ACC with ∼6.2 14 G. S. Dieckmann, G. Nehrke, S. Papadimitriou, J. Göttlicher,

H2O per CaCO3 can be synthesized at 2 °C and it transforms R. Steininger, H. Kennedy, D. Wolf-Gladrow and D. N. into ikaite via a partial dissolution–recrystallization process. Thomas, Geophys. Res. Lett., 2008, 35, L08501. More importantly, we found that ikaite can easily transform 15 C. C. Tang, S. P. Thompson, J. E. Parker, A. R. Lennie, F. into ACC when the dehydration kinetics is fast enough to pre- Azough and K. Kato, J. Appl. Crystallogr., 2009, 42, vent the nucleation of more stable crystalline phases. Our 225–233. study also provides another possibility for the transformation 16 A. Zaoui and W. Sekkal, Geoderma, 2014, 235–236, 329–333. of ikaite to glendonite, where ikaite first decomposes into 17 Z. Zou, L. Bertinetti, Y. Politi, A. C. S. Jensen, S. Weiner, L. ACC and this metastable short-lived intermediate acts as the Addadi, P. Fratzl and W. J. E. M. Habraken, Chem. Mater., precursor for the formation of calcite. Moreover, the obtained 2015, 27, 4237–4246. ACC has a very high specific surface area and a multi-level 18 S. Weiner, Y. Levi-Kalisman, S. Raz and L. Addadi, Connect. porous structure, which could have many potential applica- Tissue Res., 2003, 44, 214–218. tions such as in drug delivery,30 wastewater treatment,31 etc. 19 Y. Politi, R. A. Metzler, M. Abrecht, B. Gilbert, F. H. Wilt, I. Sagi, L. Addadi, S. Weiner and P. U. P. A. Gilbert, Proc. Natl. Conflicts of interest Acad. Sci. U. S. A., 2008, 105, 17362–17366. 20 H. Nebel, M. Neumann, C. Mayer and M. Epple, Inorg. There are no conflicts to declare. Chem., 2008, 47, 7874–7879. 21 A. V. Radha, T. Z. Forbes, C. E. Killian, P. U. P. A. Gilbert Acknowledgements and A. Navrotsky, Proc. Natl. Acad. Sci. U. S. A., 2010, 107, 16438–16443. This research was supported by a German Research Founda- 22 M. P. Schmidt, A. J. Ilott, B. L. Phillips and R. J. Reeder, tion grant within the framework of the Deutsch–Israelische Cryst. Growth Des., 2014, 14, 938–951.

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23 T. C. Council and P. C. Bennett, Geology, 1993, 21, 28 A. Mikkelsen, A. B. Andersen, S. B. Engelsen, H. C. B. 971–974. Hansen, O. Larsen and L. H. Skibsted, J. Agric. Food Chem., 24 A. L. Goodwin, F. M. Michel, B. L. Phillips, D. A. Keen, M. T. 1999, 47, 911–917. Dove and R. J. Reeder, Chem. Mater., 2010, 22, 3197–3205. 29 G. S. Dieckmann, G. Nehrke, C. Uhlig, J. Göttlicher, S. 25 J. Ihli, W. C. Wong, E. H. Noel, Y.-Y. Kim, A. N. Kulak, H. K. Gerland, M. A. Granskog and D. N. Thomas, Cryosphere, Christenson, M. J. Duer and F. C. Meldrum, Nat. Commun., 2010, 4, 227–230. 2014, 5, 3169. 30 W. Wei, G.-H. Ma, G. Hu, D. Yu, T. McLeish, Z.-G. Su and 26 A. R. Lennie, C. C. Tang and S. P. Thompson, Mineral. Mag., Z.-Y. Shen, J. Am. Chem. Soc., 2008, 130, 15808–15810. 2004, 68, 135–146. 31 E. Hautala, J. Randall, A. Goodban and A. Waiss, Water Res., 27 G. Marland, Geochim. Cosmochim. Acta, 1975, 39,83–91. 1977, 11, 243–245. Creative Commons Attribution 3.0 Unported Licence. This article is licensed under a Open Access Article. Published on 18 April 2018. Downloaded 9/27/2021 10:55:12 PM.